Arabidopsis Leaf Trichomes as Acoustic Antennae

Abstract

The much studied plant Arabidopsis thaliana has been reported recently to react to the sounds of caterpillars of Pieris rapae chewing on its leaves by promoting synthesis of toxins that can deter herbivory. Identifying participating receptor cells-potential "ears"-of Arabidopsis is critical to understanding and harnessing this response. Motivated in part by other recent observations that Arabidopsis trichomes (hair cells) respond to mechanical stimuli such as pressing or brushing by initiating potential signaling factors in themselves and in the neighboring skirt of cells, we analyzed the vibrational responses of Arabidopsis trichomes to test the hypothesis that trichomes can respond acoustically to vibrations associated with feeding caterpillars. We found that these trichomes have vibrational modes in the frequency range of the sounds of feeding caterpillars, encouraging further experimentation to determine whether trichomes serve as mechanical antennae.

Figure 1

Structures of natural and simulated Arabidopsis trichomes. (a) Given here is a UV microscopy image, showing interior wall taper. The bar is 20 μm. (b) Given here is a confocal microscopy image of a trichome stained with a pH bioreporter, tilted by compression from above. This image illustrates some of the considerable morphological variation that occurs, which was compensated by evaluating image stacks of trichomes with differing shapes. (c) Given here is a 3D illuminated rendering of the aerial portion of a trichome. (a and b) Reprinted with permission from Zhou et al. (2). To see this figure in color, go online.

Figure 2

Schematic of a model to predict the order of magnitude of the natural frequency for torsional oscillations occurring about the trichome stalk axis.

Figure 3

The first eight mode shapes for an archetypal trichome. The lowest mode involved torsion about the stalk axis, and the next modes involved flexure and distension of the stalk. In higher modes, flexure of the branches was observed. Modal shapes are better visualized through animations provided in Movies S1, S2, S3, S4, and S5. To see this figure in color, go online.

Figure 4

The lowest vibrational mode was torsional for the baseline parameters of the archetypal trichome (dashed vertical line: baseline Young’s modulus). The character and natural frequency for the first mode were largely insensitive to Young’s modulus over approximately two orders of magnitude in the vicinity of the baseline Young’s modulus. For very low Young’s modulus, the first mode switched from the torsional mode to the flexural mode shown in position (A). To see this figure in color, go online.

Figure 5

The mechanics of the leaf foundation was a strong determinant of the lowest natural frequency of the trichome. High compliance caused a switch from the torsional vibration mode to a rocking mode. The baseline parameters (dashed vertical line) provided a peak in the frequency, indicating that subtle changes such as pH-induced compliance could be used to trigger enhanced sensitivity to low frequency acoustic signals. To see this figure in color, go online.

Figure 6

The natural frequencies of the archetypal trichome decreased with decreasing turgor pressure. (Vertical dashed line) Baseline parameters. To see this figure in color, go online.

Figure 7

Effects of cell wall taper on the natural frequency of a trichome. The choice of model for the wall taper affected frequencies by up to a factor of 2, but did not affect trends. To see this figure in color, go online.